microRNAs: Key Players in Plant Response to Metal Toxicity

Abstract

Environmental metal pollution is a common problem threatening sustainable and safe crop production. Heavy metals (HMs) cause toxicity by targeting key molecules and life processes in plant cells. Plants counteract excess metals in the environment by enhancing defense responses, such as metal chelation, isolation to vacuoles, regulating metal intake through transporters, and strengthening antioxidant mechanisms. In recent years, microRNAs (miRNAs), as a small non-coding RNA, have become the central regulator of a variety of abiotic stresses, including HMs. With the introduction of the latest technologies such as next-generation sequencing (NGS), more and more miRNAs have been widely recognized in several plants due to their diverse roles. Metal-regulated miRNAs and their target genes are part of a complex regulatory network. Known miRNAs coordinate plant responses to metal stress through antioxidant functions, root growth, hormone signals, transcription factors (TF), and metal transporters. This article reviews the research progress of miRNAs in the stress response of plants to the accumulation of HMs, such as Cu, Cd, Hg, Cr, and Al, and the toxicity of heavy metal ions.

Keywords: heavy metals; miRNA; response; toxicity response; transcription factor.

Figure 1

Keyword co-occurrence graph analysis using VOSviewer software. (A) A total of 568 relevant articles were searched from academic papers over the past 10 years using the keywords miRNA, Cu, Cd, Hg, Al, As and Cr, four research centers focusing on miRNA, stress, cadmium, and strategy were formed. (B) Different colors correspond to the year in which the keywords appeared on average, and keywords with blue color presented earlier than those with yellow.

Figure 2

Schematic representation of the mode of action of miRNAs in response to Cu stress. Green boxes indicate relevant miRNAs and pathways involved in low Cu stress. SPL7 transcription factors are active and regulate miR397, miR398, miR408, and miR857, which regulate genes encoding Cu-containing proteins, including Cu/Zn superoxide dismutase (CSD), CCS1, laccase (LAC), and phycocyanin (PLC), thereby conserving Cu as essential Cu protein (such as plastocyanin). Red boxes indicate that under high Cu stress, SPL7 is inactivated, miR398 is down-regulated, and the expression of target genes CSD1, CSD2, and CCS1 is up-regulated, mitigating the threat of ROS from increased Cu content and increased Cu protein accumulation.

Figure 3

The regulatory network of miRNA target genes is involved in the response of plants to Cd stress. The blue area indicates the pathway by which miRNA participates in metal chelation. The green region represents the process by which miRNA participates in metal transport. The orange area indicates that miRNA participates in the regulation of related plant hormone signaling pathways, including auxin, jasmonic acid, and cytokinin.